Weaknesses in the reporting of cross-sectional studies according to the STROBE statement: the case of metabolic syndrome in adults from Peru.

INTRODUCTION
The inadequate reporting of cross-sectional studies, as in the case of the prevalence of metabolic syndrome, could cause problems in the synthesis of new evidence and lead to errors in the formulation of public policies.


OBJECTIVE
To evaluate the reporting quality of the articles regarding metabolic syndrome prevalence in Peruvian adults using the STROBE recommendations.


METHODS
We conducted a thorough literature search with the terms "Metabolic Syndrome", "Sindrome Metabolico" and "Peru" in MEDLINE/PubMed, LILACS, SciELO, LIPECS and BVS-Peru until December 2014. We selected those who were population-based observational studies with randomized sampling that reported prevalence of metabolic syndrome in adults aged 18 or more of both sexes. Information was analysed through the STROBE score per item and recommendation.


RESULTS
Seventeen articles were included in this study. All articles met the recommendations related to the report of the study's rationale, design, and provision of summary measures. The recommendations with the lowest scores were those related to the sensitivity analysis (8%, n= 1/17), participant flowchart (18%, n= 3/17), missing data analysis (24%, n= 4/17), and number of participants in each study phase (24%, n= 4/17).


CONCLUSION
Cross-sectional studies regarding the prevalence of metabolic syndrome in peruvian adults have an inadequate reporting on the methods and results sections. We identified a clear need to improve the quality of such studies.


Original Article
Weaknesses in the reporting of cross-sectional studies according to the STROBE statement: the case of metabolic syndrome in adults from Peru Las deficiencias en la presentación de los estudios transversales de acuerdo con la declaración STROBE: el caso del síndrome metabólico en adultos de Perú

Introduction
The inadequate reporting of biomedical research is a longstanding and potentially serious global problem that is not entirely evident to many researchers 1 . All scientific study must be fully and accurately reported, allowing a proper understanding of their methodology, findings and replication of the same if needed 2,3 . However, most of the reports are far from those ideals 2 . For this reason, many guidelines that seek to standardize and improve the reporting quality of different types of research were developed in the past few years 4 . Strengthening the Reporting of Observational studies in Epidemiology (STROBE) is a guideline whose recommendations have been established in order to adequately report observational studies (cohort, case-control and cross-sectional studies) 3,5 . It should be noted that the STROBE recommendations assess the quality of reporting, but not the research or methodological quality per se 6 .
Moreover, an inadequate reporting of cross-sectional studies could lead to problems in the synthesis and adoption of new evidence and generate errors in the justification and formulation of public policies 2 , especially in regions with limited resources like Peru or other Latin American countries. For example, the prevalence of Metabolic Syndrome (MS) is relevant to public health issues because it had been associated with an increase of two to three times the risk of presenting a heart attack or stroke 7 and five times higher risk of developing type 2 diabetes mellitus 8,9 . Nonetheless, the diversity of criteria for defining MS 10-16 associated with the poor reporting in cross-sectional studies, generate confusion when interpreting the real extent of the problem. For that reason, this study aims to evaluate the reporting quality of cross-sectional studies regarding the prevalence of MS in Peruvian adults, using the STROBE recommendations as an objective tool.

Materials and Methods
This descriptive study was carried out in two stages. First, a systematic literature search was performed to identify the articles to be included in the study. Then, the quality of the reporting was assessed using STROBE. This study followed the recommendations of the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) statement for its reporting 17 .

Search strategy
We conducted the search in MEDLINE/PubMed (1997-4/12/2014), LILACS (1982-4/12/2014), SciELO (1999 -4/12/2014), LIPECS (1987-4/12/2014) and BVS-Perú (INS, MINSA and OPS; 1997-4/12/2014) after reaching consensus regarding each database search strategy. The terms "Metabolic Syndrome" and "Sindrome Metabolico" were used in combination with the term "Peru" depending upon the database. The terms were used in english for MEDLINE via PubMed; in Spanish for LIPECS, BVS-Perú and OPS; or in both languages for LILACS and SciELO. The last search was completed on December 4, 2014. This was done simultaneously and independently by three researchers (JCT, EFR, OJP) and a list of found items was made. Then, search results were compared and no differences in the outcome were found among the three authors.

Study selection
The selection was made with the purpose of obtaining studies whose external validity allow us to extrapolate their results to different populations of Peru. The following eligibility criteria were defined: 1) population-based observational studies; 2) studies involving random sampling instead of volunteer recruitment; 3) studies that reported prevalence data of MS according to a selected criteria and 4) studies involving adults 18 years or older of both sexes. There were no language restrictions. Full-text articles were evaluated by three researchers (JCT, EFR, OJP) and those who met the inclusion criteria were selected. Additionally, a secondary search through the bibliographic references of the selected articles was made and duplicates were removed. We excluded studies involving pediatric or inpatient population, workers from any institution or patients recruited through health campaigns. Reviews, editorials or short communications were also excluded. A fourth investigator (GM) was consulted in the event of discrepancies and reached a consensus.

Instrument
We used the STROBE recommendations as an objective tool to evaluate the quality of the reports. STROBE presents 32 recommendations for the appropriate reporting of observational studies. These recommendations describe the proper way of reporting the title, abstract, introduction, methods, results, discussion and financing 5 . According to the language of each publication, we used the cross-sectional studies suggested-version, available in English 3 or Spanish 18 .
For this study, we used 30 of the 32 recommendations from crosssectional studies. We considered as not-applicable the items 16b (the limits of the ranges for continuous variables of MS -blood pressure, glucose, HDL, triglycerides, or abdominal circumference are already defined for each criterion) and 16c (the objectives of the studies were not to evaluate the report of relative or absolute risk). Additionally, two recommendations were considered as notapplicable for the following cases: 12d if the study had a simple random sampling (single-stage) and 12e if the article fulfilled 12a, 12b and 12c recommendations.

Data extraction
Two formats for data extraction were developed. The first contained information about the general characteristics of each article: first author, publication year, name of the study from which the data came from, publication language, study period, city, type of population, sampling type, age range, sample size and criteria used to define MS. The second format is a list with 30 of the 32 STROBE recommendations.
Three researchers (JCT, EFR, OJP) reviewed the full-text of the articles with their respective protocols, in case the latter were cited, and the data was extracted. Each investigator assessed whether the reports identified met or not the STROBE recommendations. We did not hide the names of the authors nor the title of the articles.
Finally, the corresponding author of each included article was contacted by email. In each email, we presented the purpose of the study and the recommendations fulfilled by the article, based on our analysis according to STROBE. This step was done in order to clarify potential disagreements with our assessment. The inputs of each author were analyzed according to the methodology described above and modifications to our analysis were performed as appropriate. In case of no response, a reminder was sent 7 days after the first email. We waited in total for 14 days for the author to reply, otherwise our analysis was considered as the final result.

Analysis
Two types of scores were reported as follows: score per article and per recommendation. The score per article was defined as the number of the STROBE recommendations adequately reported, divided by the total of recommendations applicable per article and expressed as a percentage. The score per recommendation was defined as the number of articles that met each STROBE recommendation, divided by the total of articles for which the recommendation were applicable and expressed as a percentage.

General features of the reports
Finally, regarding the criteria used to determine prevalence of MS in adults from Peru, 7 articles (41%) used the NCEP-ATP III criteria 12 , 2 the JIS criteria 16 , 1 the AHA/NHLBI criteria 13 , 1 the IDF criteria 14 , and the others used more than one criterion.
Reporting Quality according to the STROBE recommendations Thirteen (76%) out of the 17 corresponding authors answered the emails, commenting and supporting if they agreed (5/13) or disagreed (8/13) with our analysis. Most of the disagreements were found in the recommendations related to the statistical analysis (sample size modification according to the sampling strategy, and the analysis of sensitivity, subgroups and missing data) and the description of the number of participants for each study phase. Based on these disagreements, each recommendation was reviewed again and answers were sent via email with the respective modifications. Table 2 shows the number of articles that met each STROBE recommendation. The recommendations that were fully met were those related to the reporting of the reasons and rationale of the investigation (recommendation 2), to the reporting of the study design (recommendation 4) and to provide summary measures (recommendation 15). In addition, 16 out of the 17 articles adequately defined their variables and their respective measurement methods (recommendation 7 and 8). They also reported how they grouped and analyzed the quantitative variables (recommendation 11) and provided confidence intervals for their estimates (recommendation 16a). On the other hand, the recommendations with the lowest scores were those related to the description of the sensitivity analysis (recommendation 12e; 1/13 [8%]), to consider the use of a flowchart for the participants (recommendation 3; 3/17 [18%]), to explain the analysis of the missing data (recommendation 12c; 4/17 [24%]), to specify the number of participants in each study phase (recommendation 13a; 4/17 [24%]), to describe the reasons for the loss of the participants (recommendation 13b; 5/17 [29%]) and to specify the steps taken to identify possible sources of bias (recommendation 9; 7/17 [41%]). In the supplementary material shown the score assigned for each STROBE recommendation applicable per article. Only 3 out of the 17 articles met all the STROBE recommendations.

Discussion
The results of the analysis show that the fulfillment of the STROBE recommendations for the reporting of cross-sectional studies on the prevalence of MS was mixed, being the ones related to the methodology and results the lowest. These deficiencies are particularly critical for methodologically well-conducted studies and properly analyzed. For that reason, every scientific report, to be reliable, must provide a clear, complete and transparent presentation of what was planned, made and found, in order to facilitate the adequate interpretation and diffusion of their findings 3 .
Of the 17 articles involving 12,789 people, 14 (11,804 people) showed limitations when reporting the methodology related to the statistical analysis, including sensitivity analysis, missing data and sources of bias. Also, the report of the results was not clear regarding the description of the participants flow and the reasons of loss in each study phase. These weaknesses are not unique to   12e Describe any sensitivity analyses.

Participants 13a
Report numbers of individuals at each stage of study-eg numbers potentially eligible, examined for eligibility, confirmed eligible, included in the study, completing follow-up, and analysed 4 (24) 13b Give reasons for non-participation at each stage. 5 (29) 13c Consider use of a flow diagram.

(18)
Descriptive data 14a Give characteristics of study participants (eg. Demographic, clinical, social) and information on exposures and potential confounders.

(76)
14b Indicate number of participants with missing data for each variable of interest.

(18)
Outcome data 15 Cross-sectional study: report numbers of outcome events or summary measures.

(100)
Main results 16a Give unadjusted estimates and , if applicable, confounder-adjusted estimates and their precision (eg. 95% confidence interval). Make clear which confounders were adjusted for and why they were included.

(94)
16b  this scenario as further investigations, in fields other than MS, have used the recommendations of STROBE to analyze the report of other observational studies and had also described limitations in the same areas [39][40][41][42][43][44][45] . On the other hand, 7 (41%) out of the 17 articles were published before the creation of STROBE and this could explain their weaknesses in its reporting in contrast to those published after (average score pre-STROBE 60%; average score post-STROBE: 77%). However, it has been shown that the quality of reporting of observational studies still remains suboptimal several years after the creation of STROBE 46 and that, despite some authors refer to follow the recommendations of STROBE, more than half do it inappropriately 6 . Still, 3 articles (985 people) 30,32,35 mentioned using STROBE to write its report and when analyzed, it was certified that they met all recommendations.
The elaboration of an optimal research report is responsibility of the main authors, but several mechanisms (editorial policies editorial board, external reviewers) play a role in the process of publishing and also aim to an appropriate report 47 . In order to achieve this objective, biomedical journals should adhere to reporting guidelines such as STROBE; also, editors and reviewers should be trained to demand its proper use 2 . In the case of biomedical journals in Latin America and the Caribbean, only 28% recommends on its website any specific guideline to improve the quality of reporting 47 . In this instance, although we have no data regarding the editorial policies of the journals at the time of publication of the selected articles, currently 43% of the 14 journals (2 of 3 peruvian journals and 4 of 11 foreign journals) suggest the authors to follow the STROBE recommendations as an editorial policy. The quality of reporting of observational and cross-sectional studies could be improved if journals introduce an active policy of adherence to reporting guidelines such as STROBE 46,48 .
Furthermore, an open access initiative that seeks to spread this kind of reporting guidelines is the EQUATOR Network 49 (http:// www.equator-network.org/).
Even though there are barriers to provide more details of what has been done and found, such as the article's length allowed in biomedical journals or the cost of its publication, the prior publication of the study protocol or the publishing of supplementary data online (eg. www.figshare.com) are some alternatives to overcome these limitations.
Considering the above, it should be noted that the scientific reports play a greater purpose in addition to the generation of new knowledge. In particular, epidemiological studies have different audiences, uses and implications. For a more technical audience, studies should report detailed estimates of the burden of the diseases that allow prioritization of public policies. On the other hand, in case of a more general audience, they should provide a consistent message about a particular situation. On both platforms, technical and general audiences, we found that the articles analyzed regarding MS in Peru have significant restrictions in its report that limit the appropriate use of their findings.
The limitations of our study are that some of our results might have been different if they were assessed by other researchers, however, to avoid subjective decisions, each corresponding author was contacted to verify our analysis, obtaining a high rate response (76%). Furthermore, we can not assume that every STROBE recommendation has the same impact on the quality of the report, thus assigning an equitable score to each recommendation could be considered as arbitrary. However, we decided to use this strategy to help readers have a global view of the quality of the reports.